Darren Naish: Tetrapod Zoology

"It is the best zoological blog out there, period"

Wednesday, June 28, 2006

British eagle owls: an update

Yesterday I visited Bernie to compare dead stag beetles (go here for more on this) and to collect both my dead Fire salamander Salamandra salamandra, and an assortment of old stuffed birds (all of which are needed for a project on foot claw morphology: more on that in the future). While at his house I noticed that the February edition of Bird Watching magazine – which I often look at in the shops but never buy – includes an article by Adrian Thomas on Eagle owls Bubo bubo in Britain. The cover states ‘What is Europe’s top hunter doing in the UK?’. An article on British eagle owls has also recently appeared in The Palaeontological Association Newsletter (McGowan 2006) and several web sites, including those of the RSPB and World Owl Trust (WOT), have also provided new, updated information on this subject within recent months. In a previous post I introduced this subject, and because new information is now available, it’s an appropriate time for an update.

In the previous post I noted how a recent BBC TV programme (which I now learn was titled Return of the Eagle Owl) made the incredible claim that there might be as many as 500 pairs abroad in this country. Unfortunately I missed the relevant programme, and this claim came to me as a pers. comm. from someone who saw it. Well, here’s a good demonstration of why you shouldn’t necessarily trust pers. comms. Read on.

The best known British eagle owls are a pair in the Yorkshire Dales that successfully bred on Ministry of Defence land in the spring of 2005. They’ve actually been breeding since 1997, or possibly 1996, and have managed to raise 23 chicks during this time. Thomas (2006) mentioned ‘two other confirmed breeding pairs in the UK’ (p. 13) and noted that there are possibly more, and it has also been brought to attention that pairs in Galloway, Invernesshire and Sutherland have also been confirmed as breeders. It’s unlikely that the ‘500 pairs’ is anywhere near likely therefore, nor was this figure mentioned in Return of the Eagle Owl, so don’t take it seriously!

Already some of the chicks of the Yorkshire pair have moved far afield, with one of them having been reported from Shropshire (where it was electrocuted on power lines). As Tommy Tyrberg noted in a comment on the previous post, eagle owls aren’t really birds of ‘surviving vestiges of wilderness, immune from human exploitation’ as it says in Birds of the Western Palearctic, but are actually quite happy living close to people. Populations in The Netherlands and Sweden are doing ok close to noisy quarries, in working farmland, and in and around rubbish dumps. Britain is a small place with no wilderness at all, and evidence for humans and their recent activity is everywhere, so the adaptability of the eagle owl, and its success on the continent despite human activity, certainly suggests that it’ll do fine in this country.

Having said that, in January 2006 came the disappointing news that the female of the Yorkshire pair had been killed, with its death apparently occurring just before Christmas. Autopsy showed that the shot used was large-gauge like that used to shoot foxes, and not small-gauge like that used for hunting gamebirds (thus probably ruling out a case of mistaken identity). The bird had an empty stomach, and thus may have starved to death after being shot. If eagle owls are colonising our islands naturally, this is a sad loss of an important individual. The killing may also have been illegal – ultimately this depends on whether or not the bird was here ‘naturally’ – and the North Yorkshire Police are pursuing enquiries.

Thomas (2006) also provided some new discussion on the source of origin of the British eagle owls: might they be vagrants that are naturally colonising Britain from continental Europe? He noted two pieces of evidence that might support this hypothesis. Firstly, Return of the Eagle Owl looked at the research of raptor conservationist Roy Dennis, and his examination of 18th and 19th century eagle owl records in Britain shows that the birds were mostly reported between September and January – the time ‘when one might expect vagrants to arrive’ (Thomas 2006, p. 15).

Secondly, ornithologists monitoring eagle owls in Switzerland have shown that the birds can move as far as 350 km, passing obstacles such as major mountain ranges as they go. A hop across the English Channel may therefore seem no trouble at all, and indeed we know that some European owls, like Long-eared owls Asio otus and Short-eared owls A. flammeus, cross bodies of water like the North Sea regularly.

Thomas (2006) countered that sedentary European birds seem to find the English Channel and/or the North Sea an insurmountable barrier: Black woodpeckers Dryocopus martius don’t cross the channel for example, even though their range approaches the French coastline. Similarly, Eurasian pygmy owls Glaucidium passerinum – widespread in Scandivania where they range right up to the North Sea coastline – have never colonised Britain. Ural owls Strix uralensis and Great grey owls S. nebulosa are widespread in Sweden, but also haven’t colonised Britain. Tawny owls S. aluco don’t cross the Irish Sea. However, just because these species are sedentary doesn’t mean that eagle owls have to be too. As the Long-eared and Short-eared owls show, rules on dispersal capability vary among species and there isn’t a single rule that applies to all Strigidae. The possibility that British eagle owls are natural colonisers is therefore worthy of consideration and needs more investigation.

Tony Warburton of the World Owl Trust has written a piece (go here) on the WOT’s position. They are confident that the British eagle owls are natural colonisers, and that confirmation of eagle owl breeding in Britain is news akin to that of the reintroduction of the White-tailed eagle Haliaeetus albicilla or the successful increase in Red kite Milvus milvus numbers. The WOT also contends that the British Ornithologists Union should now add Eurasian eagle owl to the official British bird list and that they should receive full protection.

What does the BOU say about this? In a 1996 review of the eagle owl’s status in Britain, they concluded that insufficient evidence was available to accept the species on the British list (they concluded that the 90 reports they examined were either not definitely of Bubo bubo, or might have been of birds that had escaped from captivity). So far as I can tell, they are watching the situation but are not yet prepared to be as positive as the WOT is about possible native status. Similarly, the RSPB is being cautious: they say that they would be more than happy to accept the species as a native, but compelling evidence that demonstrates this has yet to be produced (go here for their statement).

We have some more news on fossils. I noted in the previous post that Giles (2006) drew attention to John Stewart’s mention of possible post-glacial eagle owl fossils. In The Palaeontological Association Newsletter article mentioned above, Al McGowan (2006) also mentioned Stewart’s interest in this subject and, even better, discussed and figured an eagle owl carpometacarpus from post-glacial deposits near Cheddar, Somerset. This provides powerful support for the natural presence of the species in modern Britain (‘modern’ in the geological sense you understand). You can see McGowan’s article here.

Of course, if our eagle owls have gotten here naturally, they would be protected under the Wildlife and Countryside Act. Any impact that they have on other British animals – and as discussed in the previous post they might affect raptor numbers as well as those of Black grouse Tetrao tetrix – will be something we can record, but not intervene in. Conversely, if it can be shown that the British eagle owls were bred in captivity and later released, they don’t deserve protection and an argument could be made that they should be removed.

Given the balance of evidence, my feeling at the moment is that at least some of our eagles owls have gotten here themselves. We await further news.

Tuesday, June 27, 2006

Ichthyosaur wars and marvellous mixosaurs

Another significant hurdle: today I finished making the required changes to my thesis (should have dealt with it sooner, but you know how it is). So right now I’m feeling pretty fired up about Eotyrannus and Yaverlandia, and I really should work hard on getting the manuscripts done and submitted.

Other interesting things have been happening. My good friend Bernie Dempsey phoned me on Saturday. He’s been out filming Honey buzzards Pernis apivorus and looking for European nightjars Caprimulgus europaeus recently, but the most interesting thing is that he’s been discovering lots of stag beetles, all of them with their abdomens eaten out by some large predatory tetrapod. If this sounds familiar it’s because this formed the subject of a recent blog post (go here). We’re going to compare corpses to see if all the animals were killed the same way. The reason he was phoning was to see if I knew what was killing the beetles (I didn’t answer, but merely directed him to this blog).

I also caught up recently with my good artist/writer friend Steve White (website here). After talking about British big cats, the Sultan’s elephant and all manner of other things with him I felt especially keen to complete my post on the Cupar roe deer carcass (first mentioned in the British big cats post). It’ll follow soon. But it’s something that happened during the week (on Tuesday 20th) that’s most inspired me lately, and ironically it was a talk that I gave. How arrogant is that? The talk was titled ‘Ichthyosaurs: the Mesozoic ‘fish lizards’’.

Followers of my posts might have noted that I do quite a bit of talk-giving, usually to local natural history and geology groups. I don’t know if I do more public speaking than other academics, let alone Ph.D. students, but it sure feels like it sometimes. Then again, I don’t know any academics that are in the same situation as me (devoid of all personal finance and funding). Anyway, while this stuff is fresh in my mind I feel I may as well do a post on some of the highlights.

As I’m sure I’ve said before, in talks I like to cover things that are genuinely new to the majority of the audience. And for any group of tetrapods there are always more than enough new, exciting things to cover. So in talking about ichthyosaurs I covered the basics: stuff such as, while they hung on until as late as the early part of the Late Cretaceous, they should best be regarded as animals of the Triassic and Early Jurassic as this is when their diversity was at its peak. Stuff such as the hyperphalangy and polydactyly that evolved in the limbs of some lineages, the well-known story of how soft-tissue-bearing specimens were first discovered, and all that data from Holzmaden (and other places) on ichthyosaur birth and babies.

Exploding whales, breech babies and toxic shock

On birth and babies, I contend that not all females ‘preserved in the act of giving birth’ really were giving birth when they died. Instead these individuals may have died while pregnant, with decomposition gases later pushing unborn babies out of the cloaca. Exactly this occurs in the dead bodies of beached whales today: pregnant females may have babies protruding from the birth canal, and males often have a distended penis that, similarly, has been extruded from the body cavity by gases building up inside. Of course this leads us on to the subject of exploding whales, but we won’t go there for now. I have some nice anecdotes.

Some ichthyosaurs had breech births, as their babies are preserved protruding head-first. Here again we have an analogy with cetaceans. Baby whales and dolphins ordinarily emerge tail-first, and are thus only ‘triggered’ to take their first breath when the head emerges. But if the head emerges first, the baby drowns, and its little corpse is then lodged in the mother’s birth canal. The mother then becomes slowly poisoned as the baby decomposes wedged inside her, and she dies of toxic shock. It’s not nice, but it happens, and it’s a reasonable (albeit untestable!) speculation to think that breech-birth ichthyosaur mothers sometimes died the same way too. If I remember correctly this idea was first proposed by Deeming et al. (1996), and I’ve a feeling that Naish (1997) picked up on it.

Marvellous mixosaurs

Some of the neatest new data on ichthyosaurs comes from newly appreciated taxonomic diversity. Mixosaurs are a fairly well studied and long-known group of basal Triassic ichthyosaurs, best known for little Mixosaurus (total length c. 1.5 m) named in 1887 for specimens from Middle Triassic Europe. Mixosaurs have always been depicted as rather dull and conventional (above is Zdenek Burian's famous, but very dated, life restoration of Mixosaurus). But it now seems that at least some of them were bizarre. Really really bizarre.

Middle Triassic Europe, North America and Spitsbergen was home to the mixosaur Phalarodon, named by John Campbell Merriam in 1910. At the back of its jaws are massive, rounded crushing teeth (properly known as tribodont teeth): proportionally huge, and in fact proportionally among the biggest of any ichthyosaur. The teeth at the jaw tips were slender and subconical, so Phalarodon seems to have been a generalist, perhaps picking up small soft-bodied prey with the rostral teeth, and crushing big hard-shelled prey with the tribodont teeth further back. Incidentally, a huge percentage of Triassic marine reptiles had tribodont crushing teeth like Phalarodon, and it’s a good question as to why this was so common at the time, and so much rarer afterwards. I might cover this when I produce a post on placodonts.

What also makes Phalarodon interesting is the presence of a proportionally large sagittal crest on the back of its head. Strongly compressed laterally and projecting dorsally from the skull roof to a height similar to that of the cranium itself, it must have had an important function, but we aren’t too sure what that was. A site for muscle attachment is the most popular explanation.

Like Mixosaurus, Phalarodon wasn’t particularly big, with P. major from Germany getting to perhaps 3.5 m. But the best is yet to come. The weirdest mixosaur – and, in my opinion, the weirdest ichthyosaur – is the freakish Contectopalatus atavus. Only known from the Middle Triassic of Germany, it was a giant compared to other mixosaurs, with some incomplete specimens indicating complete lengths of 5 m. Its skull was slender-jawed and, while its many subconical teeth were blunt-tipped, it lacked the huge tribodont teeth of Phalarodon. It seems not to have gone around crushing molluscs or prey like that, therefore. It also has a sagittal crest, but it’s even more prominent than that of Phalarodon. Sticking from the top of the skull like a piece of card, the sagittal crest seems to have been flanked by shallow concavities on the skull roof. Again, all of this may have been for muscle attachment, but nobody’s really sure.

A big, mysterious and bizarre ichthyosaur, Contectopalatus was originally recognised as a new species in the 1850s, but not until 1998 did Michael Maisch and Andreas Matzke name it as a new genus (Maisch & Matzke 1998). For additional data on it, see Maisch & Matzke (2000a, b, 2001). Their reconstruction of its skull is shown above. It’s at this point that I should note that not all ichthyosaur experts agree that Phalarodon and Contectopalatus are truly distinct from boring little Mixosaurus. Ryosuke Motani has strongly disagreed with this classification, and argues that all three forms should be synonymised (Motani 1999). Indeed Motani and Maisch & Matzke differ in their opinions on so many matters of ichthyosaur taxonomy and phylogeny that we talk of the ‘Ichthyosaur wars’, though it’s not as if the workers involved would ever get physically aggressive with one another (I assume). Motani is a student of Chris McGowan, or ‘god’ as those in the ichthyosaur research community sometimes call him.

Whatever its taxonomic status, there’s no denying that Contectopalatus was unusual and interesting. This begs the question as to why it’s not better known: I have yet to see a single artistic restoration of it, for example. Back when the BBC were still deciding which animals they were going to include in the Sea Monsters series (fronted by Nigel Marven) they screened in 2003, I (via Dave Martill, one of their technical consultants) strongly recommended use of Contectopalatus. But they didn’t go with it. Shame. So there it sits, in the literature, unexploited and largely unknown.

At 5 m in length, Contectopalatus is reasonable in size for a Triassic ichthyosaur, but it’s not exceptional. The more derived cymbospondylids and shastasaurs grew to larger sizes and were also far more formidable, with their stout, keeled teeth and robust jaws indicating that they were macropredators that perhaps filled the role that pliosaurs and mosasaurs did later on in the Mesozoic. And it’s among shastasaurs that we find the biggest of all ichthyosaurs, and indeed the biggest of all marine reptiles. I was going to talk about them here, but now I can’t. I was also going to talk about the swordfish that speared Alvin the DSRV and about Excalibosaurus and Eurhinosaurus and about so much else, but it will have to wait to another time.

Naish, D. 1997. Aspects of Ichthyosaur Evolution and Ecology With Comments on Cross-Taxon Convergence Seen Throughout Marine Tetrapods. Research Project Report 1997/97, Department of Geology, University of Southampton, pp. 80.

Thursday, June 22, 2006

Hot heads and farmyard galliforms

Yesterday Will and I spent time on the farm. I scratched lots of pigs and got chewed by a goose, but the things that interested me most were the galliforms. Like my Marwell Zoo posts (go here and here), this isn't going to be one of my standard lengthy essay-type posts: more a collection of pictures, accompanied by a tiny bit of information*.

We start with Helmeted guineafowl Numida meleagris (photo at left). Guineafowl are terrestrial foragers that eat a lot of arthopods, and they've been shown to be important controllers of ticks in areas where tick numbers are high (Duffy et al. 1992). This can make them an important weapon in the fight against Lyme disease and other tick-borne diseases. What's with the cranial crest (or casque)? Conventionally assumed to be used in display and species recognition, it may in fact play an important role in keeping the brain cool, though I don't have the relevant paper to hand and can't be bothered to go dig out the reference.

* And I don't need to tell you that I wrote that before completing the post.

I spent far more time looking at turkeys Meleagris gallopavo. Male turkeys - called stags - famously display a distensible frontal process, or snood, fleshy polyp-like lumps called caruncles, and a dewlap that extends from the lower jaw to the neck. The structures are enlarged and flushed red in display, and the snood visibly extends in an excited bird. While displaying to a female or intimidating a rival a stag raises its body feathers. They will also drag their rectrices along the ground, wearing the tips off and creating a distinctive 'shuff-shuff' noise. I'm interested in those cases where birds modify their plumage by way of behaviour, and this is a great example. Rooks Corvus frugilegus and motmots (Momotidae*) are other good examples.

* Not a typo.

It figures that the caruncles, snood and wattle have evolved as display structures. Indeed some studies (and again I don't have the references to hand) indicate that females prefer stags with the broadest heads (and thus the broadest-based snoods) and Buchholz (1995) linked the appearance of the structures with parasite loads (and thus fitness).

But, like the crest of the guineafowl, could these structures have a thermoregulatory role as well? If so, it's a negative effect, with the naked skin causing the birds to overheat at times. Males seem to suffer more from heat stress than females do: they hide in the shade on hot days more than females do, and also pant more and are less keen to flee from people on sunny days than females are. It's also been shown that exposure to direct sunlight for extended periods can reduce male fertility by about 10% in domestic bronze turkeys, so sitting in the sun on a hot day is clearly not a good idea if you're a turkey. Buchholz (1996) looked at this area but noted that more study of wild turkeys was needed.

Finally, we come to chickens Gallus gallus. With my mind on naked display structures (if you'll pardon the expression) and thermoregulation, I looked at wattles and combs anew. Might the combs and wattles of chickens, which can often be proportionally large, also have a role in temperature regulation? A positive one or a negative one?

Hens were traditionally thought to prefer those cocks that are socially dominant and in possession of large combs, and several studies provide support for this. I'm interested however in Leonard & Zanette's (1998) discovery that hens prefer males that indulge in lots of wing flapping: an audible behaviour that cocks perform when courting or intimidating other males. A high rate of wing flapping presumably indicates fitness, and cocks perform it more when sexually frustrated, apparently. Interestingly, this mate selection mechanism differs from that of Red junglefowl G. g. murghi where, according to some studies, females chose mates depending on comb size and other morphological features.

But if wing flapping is so important, and if (according to some studies) comb and wattle size isn't, why possess the big comb and wattle at all? Might they be exapted for a role in thermoregulation (having originally evolved for display)? But might they actually help cocks to shed heat (like the casque of the Helmeted guineafowl), rather than allow overheating as do the display structures of turkeys? I don't know, and again I must confess to throwing stuff out there without checking the literature first. Naughty me.

Tomorrow we submit the post-review version of the British dinosaurs MS.

Dinosaurs come out to play

As a kid I always got the impression from textbooks that the only tetrapods (and thus only animals) that engage in play behaviour are (1) mammals and (2) a few really smart birds, like corvids and some parrots. Raptors are also known to engage in play behaviour, with it being relatively well documented that adults will drop feathers in front of their flying juveniles. The juveniles catch the feathers as if they’re pretend prey.

But it would seem that play behaviour is not allowed to occur in lissamphibians, non-avian reptiles, or the majority of birds. They just don’t do it, or at least no one has ever recorded them doing it. So why do mammals and oh-so-clever corvids and parrots, and predatory raptors, play, and why do other tetrapods not? Maybe so-called ‘higher tetrapods’ engage in play behaviour because full-blown endothermy allows this sort of superfluous, energy-wasting behaviour; maybe it’s a result of enhanced encephalisation; or maybe it’s only possible if extensive parental care allows juveniles enough behavioural ‘security’ to indulge in carefree behaviour.

Well, here’s the news. All of the above is crap. You might be surprised to hear that play behaviour is far from unique to mammals and a minority of birds, but has also been documented in turtles, lizards, crocodilians and even lissamphibians and fish (Bekoff 2000, Burghardt 2005). But because the reports discussing or mentioning play behaviour in these animals have been mostly anecdotal, and hence only mentioned as brief asides in larger behavioural studies or in brief one-page notes published in obscure journals, they have largely gone overlooked until recently.

Hold on: play behaviour in reptiles, amphibians and fish? Before looking at this further we need to sort out exactly what ‘play’ really is. How can it be defined? Of course this is something that ethologists have been arguing about for decades, and lengthy papers and virtually entire books (see Smith 1984 and Bekoff & Byers 1998) have been devoted to this topic alone. A rough working definition of play might be: a repeated behaviour, lacking an obvious function, initiated voluntarily when the animal is unstressed.

Most play behaviour – namely that observed in mammals and the more intelligent birds – is easily recognized by us because it resembles the sort of activities that we ourselves already recognize as playful. But this creates the obvious problem that play behaviour in other animals might be difficult to recognize because it is rather different from the sort of behaviours we ‘expect’ to represent play. Juvenile mammals tend to employ obvious honest signals when they’re playing: we’re all familiar with the ‘play face’ and bow-like action that canids (wild and domestic) use to initiate play, for example, and the play behaviour that they indulge in – chasing, play-biting, tussling and role-reversing – recalls human play behaviour.

However, if we employ the rough definition used above, behaviours reported widely among tetrapods can be seen in a new light. It turns out that several non-mammalian, non-avian vertebrates engage in repeated, apparently functionless behaviour that is initiated voluntarily in unstressed individuals. Sometimes this behaviour is directed toward inanimate objects (so-called manipulative play or object play).

Most of the key research in this area has been produced by Gordon M. Burghardt (his website is here), and if you’re interested in his research it’s worth checking out his new book (Burghardt 2005). There’s stuff here about apparent play behaviour in fish and – shock horror – even, outside of vertebrates, in cephalopods. I’m particularly interested in the play behaviour that’s now been documented in captive trionychid and emydid turtles (Burghardt 1998, Burghardt et al. 1996, Kramer & Burghardt 1998).

Thinking about this reminded me of an activity indulged in by one of the Red-eared sliders Trachemys scripta we used to have in my UOP office. One of the terrapins used to regularly remove the plastic hose from the filter box in its tank, and then nudge the filter box around the tank. This was irritating as we (we = myself and Sarah Fielding) had to keep repositioning the box and reconnecting the hose. I honestly didn’t think at the time that this behaviour ‘meant’ anything, but I’m wondering now if it was a form of play. Certainly those animals were bored with nothing to do in their little tank, so maybe they were in need of behavioural enrichment, and hence searching for objects to manipulate.

By introducing objects like wooden blocks and chains into enclosures, Burghardt and colleagues noted exactly this occurring in turtles, crocodilians and lizards. An Orinoco crocodile Crocodylus intermedius rated particularly high in terms of its response to the objects, and appeared to exhibit both curiosity and playfulness toward them. There’s also a published account of an American alligator Alligator mississippiensis exhibiting playful behaviour directed at dripping water (Lazell & Spitzer 1977), and there are also accounts of crocodilians possibly playing with carcasses, and apparently surfing in waves (go here for more on these accounts). I’ve seen a short sequence of film of two sibling Nile crocodiles Crocodylus niloticus tussling with one another in what looked like play behaviour.

The best data however comes from monitor lizards, and in fact from one individual monitor lizard in particular. Kraken is a well-studied female Komodo dragon Varanus komodoensis kept at the Smithsonian National Zoological Park in Washington, D. C. Developing a close bond with her keepers, it began to be noticed that she directed an unusual amount of curiosity toward shoe laces and to objects concealed in people’s pockets (such as handkerchiefs and notebooks). Kraken would tug at or sever shoe laces (with her teeth), and would gently pull objects out of people’s pockets. The keepers then began to introduce boxes, blankets, shoes and Frisbees into Kraken’s enclosure, and many of Kraken’s reactions would be interpreted as playful if witnessed in a mammal. Kraken has also been recorded to play tug-of-war with her keepers.

In a detailed, thorough study of Kraken’s interactions with objects and her keepers, Burghardt et al. (2002) concluded that play-like behaviour in Komodo dragons definitely meets the formal criteria for play: ‘Kraken could discriminate between prey and non-prey and showed varying responses with different objects (i.e., ring and shoe). Large lizards, such as the Komodo dragon, might be revealed as investigative creatures, and further expressions of play-type behaviors should be confirmed and explored. These findings would imply that non-avian reptiles in general and large long-lived species in particular are capable of higher cognition and are much more complex than previously thought’ (p. 116). It’s interesting to note that probable play behaviour was reported in Komodo dragons as early as 1928, incidentally. Other people have now documented play behaviour in captive monitors: for an article devoted to this go here.

So – if you’ll excuse me here for bringing in some vertebrate palaeontology - did non-avian dinosaurs play? Several authors have speculated about this, but only in fictional essays: Stout & Service (1981) depicted baby tyrannosaurs chasing, wrestling and play-biting one another, and Bakker (1995) imagined dromaeosaurids and troodontids sliding down snowy slopes in a Cretaceous winter (which explains the Luis Rey painting you can see here). Of course we don’t know whether dinosaurs played, and we never will, but given how widespread play behaviour is in living reptiles, phylogenetic bracketing indicates that at least some extinct dinosaurs almost certainly would have engaged in this. So, artists, feel free to depict baby dromaeosaurs running around with feather or stick toys in their mouths.

And, finally, here is the proof showing the tyrannosaurs really did play with micro-machines (and for details on the photo used above, go here).

Monday, June 19, 2006

More on what I saw at the zoo

Wa-hey: we have images! Here are some of the long-promised Marwell Zoo pictures I wanted to post a while back (go here). Essentially this is an assortment of some of the neatest, most exciting animals you can ever expect to see in captivity.

We start with the fossa Cryptoprocta ferox. Marwell currently has one male (the animal pictured here) and one female, and they've successfully bred them. Fossas are bizarre, looking like a mixture of cat, dog, mongoose and civet. Though classified conventionally as viverrids they are actually part of an endemic Magadascan clade located at the base of Herpestidae. They can shin up vertical poles and can also climb down, head first and with their ankles rotated somewhat. More on them another time, maybe when Mary* shows up and starts telling me about her latest adventures with lemurs. We got images of the male scent-marking a tree stump: see photo below.

* Mary Blanchard, Liverpool-based primatologist working on lemurs.

Above, the back end of an Okapi Okapia johnstoni. Marwell has lots of them, and has had breeding success. Famously discovered by Harry Johnston and named by P. L. Sclater in 1901 (Johnston thought he was tracking down reports of a new forest-dwelling equid), Okapia is a short-necked forest-dwelling giraffid, though how typical it is in the grand scheme of giraffid diversity and evolution has proved controversial. Males have short curved ossicones (so this animal is a female) that they fight with, and Marwell had (until recently) a really old gnarly male with (relatively) huge lumpy ossicones. If I remember correctly he was - at 30-something years old - the oldest okapi in captivity, and thus probably the oldest okapi in the world. They're supposed to be silent, but juveniles make coughs, bleats and other noises. Lots more could be said, they're fascinating.

Also above we have a male Greater rhea Rhea americana (also called Common rhea). Nice photo. Note the lone capybara in the background. Dave and I had a discussion today about flightlessness in ratites: a single evolution of flightlessness at the base of the clade, or multiple separate origins of it within the group? Well, that's the big question isn't it. No time to discuss it now, another time. Interesting thing about Rhea: contrary to what you might think, they apparently don't like open grassland habitat, and in the wild chose open woodland environments. Males court multiple females, get them to lay their eggs in a single nest, and then take over incubation and post-hatching duties. This form of behaviour is sort of similar to the creching present in ostriches, and the parental behaviour of male cassowaries, emus and kiwis.

Here's the male fossa scent-marking (with his anal glands). Bet you've never seen that photographed before.

Gemsbok Oryx gazella, also called Beisa oryx or African oryx. That last name is particularly stupid given that all extant oryxes are African (or Afro-Arabian if you want to be more precise). As is the case in other hippotragine antelopes, males and females look alike. All oryx are dry-adapted (as is their closest extant relative, the Addax [which they also have at Marwell]), and fantastic tales are told of their physiology. Nice pigmentation they have. This is the closest I've ever got to one.

Collared peccaries Tayassu tajacu. They have loads. Until recently there was just a single wire fence seperating the peccaries from the public, and I always thought this was a bit dangerous in view of the immense teeth these animals have. They've now installed a separate barrier fence that keeps people further back from the animals. I'd like to think this is because one of the peccaries chewed someone's arm off, but sadly I lack confirmation of this fine theory. Peccaries are omnivores, though they mostly eat vegetation (predominantly roots, fruits and tubers), and the suid-like rhinarial disk they have is obviously great for rooting in soil. They have particularly short tails (with only seven caudal vertebrae or less), hind feet strongly modified for cursoriality (some of them even lack digit II), and vertically implanted canines where the lower canine fits into a special pocket on the side of the muzzle. A similar feature is seen in hippos, so some workers think that peccaries and hippos are each other's closest relatives (which, if correct, would mean either that peccaries are whippomorphs, or that Whippomorpha is not monophyletic*). Then there's the fact that peccaries haven't always been restricted to the Americas and previously occurred in Africa.

* If you're wondering what the hell I'm talking about you'll have to wait for a future post, sorry.

There are three extant peccary species (with the third being Catagonus wagneri, a taxon only discovered in living state in 1974 - go here for more). However, Mark van Roosmalen has reportedly discovered a fourth species recently. The type specimen was eaten however. For more on this go here.

And that's that. Spent all day dealing with British dinosaurs, but you don't want to hear about that.

Friday, June 16, 2006

Basal tyrant dinosaurs and my pet Mirischia

I knew when I started this blog that my posts would be a random compilation of thoughts and observations on both living and fossil tetrapods, and I’d somehow imagined that the posts about fossil tetrapods would draw more attention than those on the living ones. I felt this prediction had come true when the post on azhdarchid pterosaurs attracted a record 14 responses.

But by and large the posts on extant animals have drawn equal amounts of praise and attention. I’m a vertebrate palaeontologist specializing in dinosaurs, but I’m as interested in living animals as I am in long-dead ones, so this is all fine by me. I do sometimes get paranoid that I’m not bigging up my own subject enough, however, and for this reason I feel pressured to produce a post on dinosaurs. And given that I have my proverbial fingers on the pulse of basal tyrant dinosaur research, they’re as good a group to examine as any.

A few introductory comments for novices before I begin. Theropoda is the group name for the predatory dinosaurs (including birds), and Coelurosauria is a major theropod group that includes birds and all the bird-like theropods (including tyrannosauroids). Tyrannosauroidea includes the familiar giant tyrannosaurs like Tyrannosaurus of the Upper Cretaceous as well as an assortment of less familiar theropods, the oldest of which are from the Upper Jurassic.

So is it time to produce the definitive blog post on Eotyrannus lengi, the dinosaur I did my phd on? Maybe. Actually, no. Eotyrannus was named by myself and colleagues in 2001, and in that initial paper we proposed that it was a basal tyrannosauroid, and one of the most basal members of the group (Hutt et al. 2001). Since then I’ve described the anatomy of Eotyrannus in full and tedious detail (the relevant thesis chapter is 118 pp and over 30,000 words long) and have come to know it well. I am now utterly convinced that it is a tyrannosauroid, and the results of my cladistic analysis (and those of others – see Holtz 2004) support this. Every dinosaur expert who knows anything about Eotyrannus agrees, by the way.

It turns out that the 2001 characterisation of Eotyrannus is horrendously wrong, as a new rigorous skeletal reconstruction (to be published soon) shows. The animal looked substantially different from the way I initially reconstructed it (see Naish 2001, Naish et al. 2001 and Holtz 2004), and in detail it’s proved to be strikingly odd and unique in many, many features. I’ll talk about these details some time soon, but not now. In fact I’m currently making arrangements to get the full monograph published in a high prestige journal, and with the co-authorship of a leading expert on tyrant dinosaurs I hope to produce an important work on tyrannosauroid phylogeny and morphology. More on this as and when it happens.

Since Eotyrannus was published a few very interesting things have been happening in the world of basal tyrannosauroids. I was aiming to discuss all of these here, but as usual I veered off at a tangent and have hardly scratched the surface. Eotyrannus seems to have been a mid-sized theropod. The type specimen is a juvenile individual that would have been 4.5 m long when complete, but fragmentary specimens from larger individuals indicate that adults were perhaps around 7 m long. But other basal tyrannosauroids are way smaller than this, mostly being less than 3 m long.

We begin with Dilong paradoxus, a basal tyrannosauroid known from excellent near-complete specimens from the Lower Cretaceous Yixian Formation of Liaoning Province, China (Xu et al. 2004). The Yixian Formation is the now famous unit that has produced all those little coelurosaurs with feathers and other integumentary structures preserved, and Dilong is no exception. It is preserved with simple quill-like integumentary structures that seem antecedent to the true complex feathers that evolved later.

Dilong has proved to be a sort of Rosetta stone for me, allowing several previously enigmatic Lower Cretaceous coelurosaurs to be reinterpreted as additional basal tyrannosauroids. Given that I haven’t published the relevant details, I’d be silly if I gave the game away here, but to be honest the only people who really care about this already know the relevant details, and furthermore I am silly anyway. The news is that a controversial little coelurosaur from the Isle of Wight’s Wessex Formation, Calamosaurus foxi (known only from two cervical vertebrae, one of them incomplete), is so similar to the cervical vertebrae of Dilong that I am confident that it too should be identified as a basal tyrannosauroid. This is mentioned in a large manuscript that came back from review some weeks ago and is currently undergoing revision, but the full story is to be revealed in a short paper that’s been completed and reviewed but now awaits post-review revamping.

I previously had Calamosaurus down as a compsognathid (Naish et al. 2001). Compsognathids are, like tyrannosauroids, basal coelurosaurs, but they retained small body size throughout their history (so far as we know). They were also conservative in all being rather alike: morphologically unspecialized with relatively short forelimbs, rather long and gracile legs and feet, and a long tail. There’s a lot more that could be said about them but this isn’t the time. Here’s the thing: the fact that Calamosaurus probably isn’t one of them after all leads us to a key question. Namely, do all the other compsognathids really go together, or is Compsognathidae as currently perceived actually an artificial assemblage of distantly related (yet superficially similar) theropods?

Back in 2004 I and colleagues named the new Brazilian theropod Mirischia asymmetrica (photo at left). That name means ‘asymmetrical wonderful pelvis’, and I think it’s a rather good descriptive name. The only known specimen really is a ‘wonderful pelvis’ (though it also includes some of the hindlimb bones), as it is 3-D and fantastically well-preserved, including even soft tissues like part of the gut and a probable post-pubic air sac (and to know the importance of that latter feature you’ll have to wait for a future post). As you might guess, it’s also asymmetrical, but I won’t talk about that here. I also don’t want to talk about the embarrassing fact that Mirischia’s generic name might imply that it was named after the fund-giving Mirisch Foundation, but (annoyingly) I only found this out after the publication of the Mirischia paper.

Anyway, Mirischia is enough like Compsognathus – particularly in the detailed anatomy of its pubis – for me to convince myself that it must belong together with Compsognathus in a little clade, and by definition this clade has to be called Compsognathidae. So in the 2004 paper, Naish et al. argued strenuously that (1) there is a little clade called Compsognathidae, the members of which can be united on the basis of shared derived characters, and (2) in addition to Compsognathus, this clade includes Sinosauropteryx and Mirischia. This published opinion is in part the result of a long series of to-ings and fro-ings between myself and my good friend Nick Longrich, for Nick has long been a vocal opponent of the idea that Compsognathidae really is monophyletic. Nick thinks that some so-called compsognathids are basal maniraptorans, and that others aren’t even coelurosaurs, but to date he’s only published an abstract on this (and to see why this is interesting and important you’ll have to wait until yet another future post. Think alvarezsaurids and stagodontids). Alas poor Longrich, surely he can’t be right. By the way, if you’re at all interested in what Nick looks like, click here. Sorry Nick.

Here’s where we bring Dilong back in. The pelvic anatomy of Dilong – an undoubted basal tyrannosauroid – is (like that of Mirischia) rather like that of Compsognathus. This is disturbing, as it all but destroys the reasons for thinking that Mirischia can only be a compsognathid. Might it actually be a basal tyrannosauroid? This has implications for another supposed compsognathid: the Isle of Wight taxon Aristosuchus pusillus (photo at left, with interpretative restoration below) which, again, I’d previously identified with confidence as a close relative of Compsognathus (Naish 2002, Naish et al. 2001, 2004). So we can now doubt that those ‘compsognathids’ known only from pelvic material really truly are compsognathids. Again, this is an idea that I’m mentioning in that large in-preparation manuscript.

In my thesis I tried to test all of this: I included all of the relevant taxa (except Aristosuchus, as I decided it wasn’t complete enough to code) and all of the characters that have been used in this debate. And the result? Well, yes, there was a monophyletic Compsognathidae, but it consisted only of Compsognathus and one other taxon (and I’d rather not say which taxon that was right now). It wasn’t Mirischia, as this came out as… a basal tyrannosauroid. Two characters helped pull Mirischia into Tyrannosauroidea. One of these was discussed in the Naish et al. (2004) paper but the other was previously overlooked. I’ll not mention them here for fear of giving away all the secrets.

Furthermore, other supposed compsognathids did not group with Compsognathidae proper. Instead they were scattered about the base of Coelurosauria. So right now – while further work and further testing and further incorporation of data is needed – I am thinking that Nick was right, and that Compsognathidae in its old, inclusive sense is an artificial grouping.

People sometimes ask what sort of relevance stuff like this really has for our understanding of animals and their evolution. Well, it actually tells us an awful lot of stuff about patterns and trends. If so-called compsognathids – all of them relatively small, ecologically and morphologically generalized, long-limbed, long-tailed theropods that hunt small vertebrate prey – are not a clade but are actually scattered about the base of the coelurosaur family tree, this likely indicates that this ecotype was the ancestral one for coelurosaurs. We might already have thought that based on other lines of evidence, but this would help confirm it. There are indications that ‘compsognathids’ could make a living just about anywhere (for reasons that, again, I’ll have to cover in another post), and if this is valid then again we have another really interesting discovery about evolution at the base of Coelurosauria.

And I’ll have to stop there. I was planning to discuss the Jurassic basal tyrannosauroids Aviatyrannis (from Portugal) and Guanlong (from China). Another time. To readers who already knew all of this stuff, I apologise. To those who didn’t: welcome to the fantastic world of dinosaurs! More to come. For the latest news on Tetrapod Zoology do go here.

Wednesday, June 14, 2006

What killed the stag beetles?

Britain’s largest beetle is the Stag beetle Lucanus cervus, a lucanid beetle that can reach 55 mm in total length. Yes I am aware that beetles aren’t tetrapods, but bear with me here. This evening I was surprised to discover, in my mother-in-law’s garden, the mangled remains of at least six adult male stag beetles, all of them clearly predated by a tetrapod, and all of them exhibiting distinct puncture marks on their elytra. Most individuals consist of an undamaged head, thorax and limbs, and it’s the abdomen that’s been eaten. All the corpses were scattered about an area of about 3 square m of lawn, with five of the six being discovered in the well-vegetated borders surrounding the lawn. So the mystery is: who dunnit?

I’ll start by stating that the garden where the beetles were found is smack in the middle of suburbia. We are not talking here about a place in the countryside, or anywhere that is adjacent or even close to any wilderness areas. It’s all built up, with various busy roads. Wildlife is actually thin on the proverbial ground.

At this time of year stag beetle males are out and about, flying around in search of mates. They are not clambering around on trees or spending much time on the ground. Could an airborne predator therefore have been responsible? Bats are out, as the only bats in the area are pipistrelles Pipistellus*, and they are way too small to tackle stag beetles (if you like bats see the previous posts: one on Greater noctules, one on Ghost bats).

* There are three species in Britain: Nathusius’ pipistrelle P. nathusii, the 45 kHz pipistrelle P. pipistrellus and the 55 kHz pipistrelle P. pygmaeus.

So what about birds? I am hard pressed to work out whether the damage present on the beetle elytra looks like it was caused by mammalian teeth or by an avian bill. Some of the specimens have a distinctly ‘chewed’ look, with punctures and dents matching the damage I’ve seen on bones and other objects chewed on by carnivorans. But others (see the close-up photo*) have puncture marks that just might have been caused by a bird. If it was a bird, it was a big, greedy one, and one that did all of its hunting during the evening or at night (as this is the only time when stag beetles fly). This makes corvids, woodpeckers and raptors unlikely to have been the predators, and in fact the close proximity of the dead beetles makes a bird predator unlikely.

* Nope. Can't get blogger to upload it.

I suppose some owls might eat stag beetles: the only own in the area is the Tawny owl Strix aluco. It’s difficult to think that an individual would consume so many big beetles in the same area, or leave the half-eaten bodies in borders around a lawn. Furthermore, there are no overhanging perches at all (there are no big trees at all in the vicinity), nor is there evidence for owls in the form of pellets or droppings.

Finally we come to terrestrial mammals, and I think this is where the true culprit must be found. Rodents are out: it’s feasible that Brown rats Rattus norvegicus would eat stag beetles, but rodent gnaw marks do not resemble the dents and punctures seen on the elytra in the least. Mustelids are out as, again, there are none in the area at all, and this goes even for badgers Meles meles which will eat stag beetles given the chance. Hedgehogs Erinaceus europaeus are definitely in the local area (go here to see how I know this: we live less than 1 km from my mother-in-law’s house), but I find it hard to imagine that they might catch so many individuals of a beetle that is not blundering around at ground level during the night. Hedgehogs can climb, but they aren’t in the habit of leaping 2 m off the ground or jumping from garden fences to catch airborne insects.

So this only leaves domestic cats Felis catus and foxes Vulpes vulpes. Both animals are big enough and agile enough to track and catch big flying insects. Cats will eat anything, including stag beetles, but I find it hard to accept that even the greediest cat would catch and consume six large beetles in the same small area. So we come to foxes. Neither the fox literature (Lloyd & Hewson 1986, Mcdonald 1987) nor the more general literature I have to hand on British mammals (Pitt 1944, Lawrence & Brown 1973, Freethy 1983, Matthews 1989, Macdonald 1995) mentions the stag beetle as a possible prey item of the fox, but then foxes will eat pretty much anything. They are also enterprising enough to exploit a new and locally abundant food source, are easily large enough to process even giant beetles, are mostly nocturnal, and will bring prey to the same place to eat it.

So that’s my conclusion. I’m not committed to this hypothesis but feel it best fits the evidence. I’d welcome any comments or better ideas, and if stag beetle predation like this turns out to be a novel observation I’ll see if I can get it published. The beetles have been retained in my personal collection of dead stuff.

It’s funny how much stuff there is to find if you only go out and look for it. For the latest news on Tetrapod Zoology do go here.

Sunday, June 11, 2006

Greater noctules: specialist predators of migrating passerines

Yesterday I assisted my brother in sorting through old piles of bricks at the back of his garden. They’d become home to a million spiders, including some of the largest Tegenaria I’ve ever seen, and as I picked up and gently squeezed a Dysdera between my (gloved) fingers I watched it bite into the material with its massive, tremendously powerful fangs (it ordinarily eats woodlice, hence those big fangs). And as I sat in the evening in his garden, I watched pipistrelle bats flying overhead, the first time I’ve seen bats in the wild in many months. It’s funny how things work out.

In the previous post I discussed bird predation in the megadermatids (the false vampires or yellow-winged bats). Here, we’re going to look at the bird predation recently documented in another bat group, the vespertilionids (vesper bats). To those of us living in the Northern Hemisphere, vesper bats are usually the most common and familiar of bats, and because they’re generally small, inoffensive, insectivorous bats, the idea that some of them might be bird predators may seem pretty radical.

Noctules (Nyctalus) are a group of Eurasian vesper bats closely related to little yellow bats (Rhogeesa), big-eared brown bats (Histiotus) and little brown bats (Myotis) (Jones et al. 2002). Six species are currently recognized, although a few additional species are included by some experts in this genus as well (Nowak 1999). Mostly dwelling in forests, they are large (body lengths 50-100 mm, forearm lengths 40-70 mm) compared to pipistrelles and other typical vesper bats, and with sleek fur that ranges in colour from golden to dark brown. Some species are migratory and make journeys of over 2300 km. They eat relatively large prey, being particularly fond of beetles, and Nowak (1999) mentions a remarkable case where a Eurasian noctule (N. noctula) was observed to catch and eat mice. The species we’re interested in here, the Greater noctule N. lasiopterus, is mostly western European but also occurs as far east as the Urals, and as far south as Libya and Morocco. It isn’t well known, and is also rare.

To better understand the ecology and behaviour of this species, Ibáñez et al. (2001) netted individuals and recorded their wing morphology, and also recorded echolocation calls from the field. Greater noctule wing morphology indicates fast flight in open areas, as they have high wing loading and high aspect ratios. This is quite different from what’s seen in the megadermatids and nycterids I discussed in the previous post where ground- and foliage-gleaning are employed to find and catch prey, and where prey are often hunted from perches. These bats use low wing loadings and low aspect ratios to practice slow, manoeuvrable flight as they glean for mostly terrestrial prey in cluttered habitats.

The echolocation calls of the Greater noctule, being long in terms of pulse duration with a low frequency and narrow bandwidth, are suited for long-range target detection in open air. This technique is quite different from the prey detection style usually employed by vesper bats: a technique suited for short-range prey that are detected in cluttered habitats.

So, both wing morphology and echolocation style indicate that Greater noctules chase and catch flying prey in the open. But what are they chasing and catching? Ibáñez et al. (2001) found that feathers made up a significant component of the bat’s droppings during March-May and again during August-November: those parts of the year when migrating birds pass through the Spanish study area. Both the proportion of feathers in the droppings, and the proportion of captured Greater noctules that produced feather-filled droppings, showed that Greater noctules must capture and eat large numbers of migrating passerines. Bird predation was first documented in this species by Dondini & Vergari (2000), and judging from later comments in the literature it doesn’t seem that they got the credit they deserve for this discovery.

Unlike those of megadermatids (see previous post), Greater noctule roosts are never littered with bird remains (which partly explains why this behaviour was overlooked for so long). Ibáñez et al. (2001) did find fresh, recently cut passerine wings (of a Robin Erithacus rubecula and Wood warbler Phylloscopus sibilatrix) underneath the bats they were netting, and they also found Robin feathers adhering to the claws of one of the captured bats. It seems that Greater noctules catch, overpower and eat the passerines during flight, just as other vesper bats do with flying insects. Greater noctules are clearly large enough and powerful enough to do this: they weigh in at about 50 g and have a wingspan of 45 cm (making them the largest of Europe’s bats). For comparison, a European robin weighs c. 20 g (though this goes down to c. 15 g after migration) and has a wingspan of 20-22 cm.

Unsurprisingly, this idea has been regarded as controversial and doubtful by some. Bontadina & Arlettaz (2003) argued that the passerine-catching idea was so unlikely that it couldn’t be regarded as correct (excellent use of logic there). They also noted that other noctule species prey on insects and not birds, and that, suspiciously, Greater noctule droppings lack bird bone fragments. None of these arguments count for much. Bird bone fragments in fact are present in Greater noctule droppings, as was reported by Dondini & Vergari (2000), who even subjected the bone fragments to SEM observation to determine conclusively their avian origin (strangely, Ibáñez et al. (2001) did not report the discovery of bone fragments, and Bontadina & Arlettaz (2003) didn’t cite Dondini & Vergari’s (2000) discovery of them). The fact that other noctules don’t hunt passerines means nothing.

Anyway, how did Bontadina & Arlettaz (2003) account for the presence of all those feathers in the Greater noctule droppings? They proposed that the bats regularly eat falling feathers, mistaking them for flying insects! That’s pretty incredible, and arguably more amazing than the idea of predation on passerines. Two responses to Bontadina & Arlettaz’s article were published (Ibáñez et al. 2003, Dondini & Vergari 2004), and both showed that the scepticism was unfounded. The case for passerine predation in Greater noctules is pretty compelling. Note to wildlife camera-people reading this: someone should try and film this behaviour, though for obvious reasons no-one’s even observed it yet (to my knowledge).

So Greater noctules are specialist predators that exploit nocturnally migrating passerines, and to date they are the only animals known to do so. There are diurnal raptors (notably Eleonora’s falcon Falco eleonorae and Sooty falcons F. concolor) that specialize on migrating passerines, but nothing else that makes a point of catching those passerines that migrate at night. Dondini & Vergari’s paper ‘Carnivory in the greater noctule bat (Nyctalus lasiopterus) in Italy’ and Ibáñez et al.’s paper ‘Bat predation on nocturnally migrating birds’ therefore have to be two of the most remarkable recent publications in the annals of bat science, and this is a field where lactation in males (Francis et al. 1994), ultraviolet vision (Winter et al. 2003) and the re-evolution of running (Riskin & Hermanson 2005) have recently been reported.

Of course bats don’t have it all their own way against birds. Raptors and owls are important predators of bats and some studies suggest that owls may account for as much as 10% of annual bat mortality (Altringham 2003). Some raptors are bat-killing specialists, like the Bat kite (or Bat hawk) Machaerhamphus alcinus of tropical Africa, SE Asia and New Guinea, and the South American Bat falcon Falco rufigularis. In fact raptor predation seems to be so important to bats that it appears to explain why bats don’t fly more during the daytime (Speakman 1991) and it may also explain why bats became nocturnal in the first place (Rydell & Speakman 1995). On the subject of raptors vs bats I was amused to see, in John Altringham’s Bats: Biology and Behaviour, a drawing of a Harrier hawk Polyboroides typus using its flexible ankle joint to probe into a cavity where some molossid bats are roosting (p. 221) (go here for more on Polyboroides).

Finally, if you're interested in bats please check out my post on vampires.

Saturday, June 10, 2006

Chewed bones and bird-eating microbats

One of the several children I was looking after yesterday knocked over a tray of rabbit bones I’d left to bleach in the sun. The bones came from a fox’s cache I’d discovered in a supermarket car-park, and as I picked them up off the ground the gnaw marks and missing ends of one of the long bones reminded me of a fascinating subject that I wish more people knew about. Not fox predation on rabbits, no, but bat predation on birds.

I’m planning to post various entries on bats at some stage (including on New Zealand’s mystacinids, recently discovered European bats, and on megabat evolution), but haven’t gotten round to it yet. As is arguably also the case with rodents, lizards or passerines, there’s enough interesting stuff to say about bats for one to become occupied with them full-time, such are their numbers (over 1000 species) and diversity. And among that diversity are a couple of lineages that have experimented with predation on other tetrapods, and I’m not talking about vampires (but I will another time).

Megadermatids, the false vampires or yellow-winged bats, are a group of the Old World and Australasian tropics. The best known members are the Australian false vampire or Ghost bat Macroderma gigas and the two Asian false vampires of the genus Megaderma. Long thought to be blood-feeders, megadermatids are odd in lacking upper incisors, and in having strongly reduced, thread-like premaxillae. They’re big, with Macroderma weighing up to 150 g and having a wingspan of 60 cm. Nycterids, the mostly African slit-faced bats, will also prey on tetrapods (frogs, birds and smaller bats). Phyllostomids, the New World leaf-nosed bats, include the tetrapod-eating genera Vampyrum, Trachops (famous for being a specialist predator of singing frogs) and Chrotopterus. They’re superficially like megadermatids, and even bigger, with Linnaeus’ false vampire Vampyrum spectrum having a wingspan of about 1 m (making it the largest microbat).

A few other tetrapod-eating bats can be found in other microbat clades, like Vespertilionidae (more on them in next post). A few pteropodids (fruit bats), notably the Hammer-headed fruit bat Hypsignathus montrosus, have been reported to feed from carrion and even attack tethered chickens (Hill & Smith 1984), and the New Zealand mystacinids are also known to sometimes scavenge from carcasses.

The foraging and predation techniques used by megadermatids have been reasonably well studied. They do eat invertebrates, but a proportion of their diet is made up of mammals (including rodents and other bats) and birds, and they also eat frogs and fish. Of all bats, megadermatids perhaps have the most flexible foraging style. They use low intensity, broadband FM echolocation calls, but also listen acutely with their massive ears for prey-generated noises, and they may also hunt prey by sight. Altringham (1999) drew attention to this possibility, noting that the eyes of some species ‘are almost owl-like’ (p. 219).

Using steath and darkness while hunting, they fly slowly among trees and shrubs and rocky areas, often close to the ground. Their attack on a tetrapod is culminated as the bat drops onto the prey, encases it in its wings and bites it hard on the head or neck (Kulzer et al. 1984). The prey is then carried back to the roost where it is eaten, and they can carry prey weighing about 60% of their own body weight. Mammal prey are usually eaten entirely, with just bits of the skull and parts of the gut, legs and tail being dropped to the floor. The situation with birds is somewhat different however, and went mostly unstudied until Walter Boles (an Australian palaeornithologist) produced a detailed paper on bird predation as practiced by the Ghost bat Macroderma gigas (Boles 1999).

The documented bird prey of Macroderma includes some 50+ species, most of which are ground-foraging passerines. Owlet-nightjars seem to be important prey items. In contrast to what happens with mammal prey, birds aren’t eaten whole. Damage to the posterior part of the sternum shows that the bats eat tissue from the abdominal region, and leave the area around the anterior part of the sternum and the coracoids alone. The distal parts of the wings and legs get dropped intact and undamaged, as do remiges and rectrices. Humeri seem to get chewed up and eaten (Boles 1999).

Given that Boles is a palaeornithologist, you should now be wondering why a specialist on fossil birds was so interested in the behaviour of an extant bat species. One of the most famous Cenozoic fossil sites in the world is Riversleigh in north-west Queensland (see Archer et al. 1996 for outstanding coverage of the whole fauna). Numerous bird fossils are known from Riversleigh, including ratites, dromornithids, storks, rails, raptors*, parrots, kingfishers, swifts and passerines (including logrunners and lyrebirds).

* Pengana robertbolesi, a Riversleigh raptor named by Boles (after his father), is yet another raptor that convergently evolved a hyper-mobile tarsal joint like that of Polyboroides (Boles 1993). If this interests you go here.

The bat fauna discovered at Riversleigh is also diverse: literally millions (according to Archer et al. 1996) of bat bones are known from there, representing (as of 1996) ‘more than 35 different kinds of bats’ (p. 135). Interestingly, at least five of them are megadermatids. And what’s really interesting is that many of the Riversleigh bird bones represent those same skeletal elements that megadermatids drop from the bird carcasses they eat, and possess damage matching that caused by megadermatids. It therefore seems that megadermatids were important accumulators of the avian remains discovered at Riversleigh (Boles 1999, p. 88).

It’s well known that owls are important accumulators of vertebrate remains, particularly in caves, but this is the first study showing that bats play this role as well. Given that, as discussed above, there are other tetrapod-eating bats elsewhere in the world, it would be interesting to know if these species also produce piles of bones beneath their roosts. I wonder if anyone has looked.

Megadermatids are well known as predators of smaller tetrapods, so no one would be really surprised to hear about any of the stuff I’ve just discussed above. But you might be surprised to learn, as I was, that an inoffensive little vespertilionid is also an awesome tetrapod predator. That’s what we’ll be looking at in the next post. PS - for the latest news on Tetrapod Zoology - including posts on vampire bats - do go here.

Friday, June 09, 2006

The kipunji, and new light on the evolution of drills, mandrills and baboons

In the previous post I discussed the Highland mangabeyLophocebus kipunji, a new monkey whose discovery is an interesting and controversial story. Though initially described only from photos, and not from a museum-accessioned specimen, a sub-adult male was found dead in a trap in August 2005, and is currently accessioned at the Field Museum of Natural History, Chicago. Study of its DNA sequence data has provided new information on the affinities and evolution of the Highland mangabey, and on mangabeys and their relatives as a whole, and this is what we’re going to look at here.

Mangabeys are an entirely African assemblage of cercopithecid monkeys, traditionally grouped together in the genus Cercocebus Geoffroy Saint-Hilaire, 1812. They’re all superficially alike, being long-tailed and long-limbed, and with moderately long muzzles and large incisors. However, molecular studies have consistently found mangabeys to be diphyletic, with the six terrestrial mangabey species forming a clade with drills and mandrills (and with macaques too in some studies), and the two arboreal mangabeys forming a clade with baboons and geladas.

The two kinds of mangabeys also differ from one another in many morphological details. Consequently, it has been widely agreed that the two arboreal species should be split from Cercocebus and given their own genus, Lophocebus (originally coined by Palmer in 1903 to replace Semnocebus Gray, 1870. The latter needed replacing as it was preoccupied by Semnocebus Lesson, 1840, a name now regarded as a junior synonym of Avahi Jourdan, 1834). I like Jonathan Kingdon’s use of the term ‘drill-mangabey’ for the terrestrial Cercocebus species, and of ‘baboon-mangabey’ for the arboreal Lophocebus species, and I’ll use them from hereon. Incidentally, drill-mangabeys are sometimes called eyelid monkeys because of their white upper eyelids, and baboon-mangabeys are sometimes called black mangabeys, for the obvious reason. This division of the mangabeys has been mostly accepted by mammalogists, but not universally so (McKenna & Bell 1997 still treat all mangabeys as the single genus Cercocebus, for example).

If correct, this diphyletic take on mangabey affinities would mean that geladas, baboons, drills and mandrills do not form a clade of ‘dog-faced cercopithecids’ as conventionally thought.

Apparently good morphological support for the non-monophyly of mangabeys came from Fleagle & McGraw’s (1999) study. They found that drill-mangabeys and drills and mandrills shared numerous features that aren’t present in baboon-mangabeys and baboons. In the humerus, drill-mangabeys, drills and mandrills share a notably broad deltoid plane, a proximally extended supinator crest, a broad flange for the brachialis, and a narrow olecranon process with a deep lateral ridge, and there are also characters in the radius and ulna that unite these monkeys to the exclusion of their close relatives. Drill-mangabeys, drills and mandrills are also united by particularly large, rounded posterior premolars, a robust ilium, a reduced gluteal tuberosity on the femur, sharp borders to the margins of the patellar groove, and other characters.

So that’s a pretty impressive list of characters, but note that they’re all associated with the terrestrial foraging style that these monkeys employ. Drill-mangabeys, drills and mandrills search manually through rotten wood and leaf litter, consuming hard nuts and seeds, and audibly cracking them with their large teeth. Furthermore, outgroup comparison (with macaques, for example) indicates that some of these characters are primitive for the cercopithecid clade that includes these species (Papionina). If we only had this morphological data, the possible monophyly of a drill-mangabey + drill/mandrill clade would be suspicious (Fleagle & McGraw 1999). But of course we don’t just have this morphological data, we also have the molecular data discussed above. So things are looking pretty robust.

And this is where the new data from that Chicago specimen of the Highland mangabey comes in. Its genetic sequences independently confirm the relationships indicated by previous molecular studies, and by Fleagle & McGraw’s morphological characters. Though initially described as a third species of baboon-mangabey (Jones et al. 2005), the Highland mangabey’s DNA show instead that it is closer to baboons that it is to baboon-mangabeys, yet it lacks the characters that unite all baboons proper. It therefore needs to be recognized as a new genus, and accordingly it’s now known as Rungwecebus kipunji Davenport et al., 2006. These authors proposed that members of Rungwecebus should now be referred to as kipunjis, and not as mangabeys anymore. Within Papionina, Rungwecebus and Papio form a clade, and the Rungwecebus + Papio clade forms a trichotomy with baboon-mangabeys and geladas. The sister-group to this kipunji/baboon/gelada/baboon-mangabey clade is the drill-mangabey + drill/mandrill clade (Davenport et al. 2006).

Given that we now have dog-faced monkeys variously scattered about a phylogenetic tree that also includes shorter-faced baboon-mangabeys, drill-mangabeys and the kipunji, you should now be wondering about the polarity and evolution of the long muzzle and large body size seen in mandrills, baboons and geladas. Is the long muzzle and large size primitive for this clade, or have these features evolved convergently two or even three times? At the moment, we can’t be sure: if the long muzzle evolved at the base of Papionina, three reversals to the short-snouted condition must have occurred, but if basal members of Papionina were short-snouted, you need either two or three independent acquisitions of the long-snouted condition. Neither scenario is clearly more parsimonious than the other.

Kingdon (1997) argued that the skull morphology of the drill-mangabeys indicates that they are dwarfed, short-faced descendants of large drill-like ancestors. Do fossils help? They might, as there are assorted fossil papionins, some of which (like Pliopapio) are long-snouted, others of which (like Parapapio) are relatively short-snouted (Frost 2001, Leakey et al. 2003). Unfortunately the phylogenetic affinities of these fossil taxa remain contentious.

What’s nice about this whole mangabey-kipunji-baboon subject is that it illustrates a point I’ve been planning to make for a while: namely, that fossils are sometimes all but useless in determining evolutionary relationships, and we most certainly don’t require them in order to uncover phylogenetic patterns. Contrary to what lay-people (and creationists) seem to think, you do not need fossils in order to uncover and reveal the reality of evolution, and even if fossils didn’t exist, scientific logic would lead us to conclude that organisms changed over time.

Don’t get me wrong, fossils are great (err, I am a palaeontologist if I remember correctly), and they can certainly elucidate and inform us about evolution and past diversity, but it’s living organisms, not dead ones, that provide the best evidence for evolutionary change.

I was hoping to cover in this post the rise and fall of the geladas, giant fossil baboons, swamp monkeys, talapoins, and the diversity of macaques. Another time I guess.

Sorry about the toys, it seemed like a good idea at the time. But how many zoologists do you know with both toy baboons and mandrills in their collection?

Thursday, June 08, 2006

The interesting and contentious discovery of the kipunji

Monkeys are one of the most misunderstood and mischaracterized of all mammals, at least among those who aren’t primate specialists. ‘Monkey’ is itself a loose term used for those members of Anthropoidea that aren’t hominoids, and here we’re only interested in the Old World monkeys (cercopithecoids).

Pet peeve no. 375 is the fact that people think that apes evolved from monkeys (they didn’t: hominoids and cercopithecoids are sister-taxa within the anthropoid clade Catarrhini*), and that apes are therefore somehow superior to monkeys in morphology and adaptability. If anything it’s the other way round, with a phenomenal post-Miocene radiation of monkeys pushing the previously hyper-diverse apes into the shadows. That’s a story for another time however.

* Having said that though, given that people have applied the term ‘monkey’ to all extant non-hominoid anthropoids, a stem-group hominoid would still likely be identified by people as a ‘monkey’.

One monkey in particular has been the focus of a lot of attention lately, the Highland mangabey Lophocebus kipunji (although this is not its current name: see next post).

The story of the Highland mangabey’s discovery is an interesting one. In January 2003 Tim Davenport of the Tanzanian Wildlife Conservation Society ‘heard rumours [from the local Wanyakyusa people of the Mount Rungwe region] about a shy and atypical monkey known as Kipunji’ (Beckman 2005, Jones et al. 2005, p. 1161), and became interesting in tracking down the species that might lay at the bottom of these reports. Meanwhile, another primatologist – Trevor Jones – had been amazed to observe an unusual, unidentifiable monkey in the Tanzanian Ndundulu Forest Reserve, a location about 350 km away from the source of the Kipunji reports.

So, at this stage, we have an ethnoknown primate known only to scientists by way of fleeting observations. This makes the Kipunji a bona fide cryptid, and, to repeat a point I’ve made before (in connection with the Odedi, a cryptic warbler from Bougainville Island), one would be justified in arguing that Davenport, Wood and their colleagues were now engaging in cryptozoological research. By definition these primatologists are therefore part-time cryptozoologists, whether they like it or not.

Good observations were finally made of the Kipunji in December 2003, and it now turned out that a monkey population reported in 2001 from the Ndundulu Forest Reserve, misidentified as Sanje mangabeys Cercocebus sanjei (itself only discovered in 1979), were actually reports of the Kipunji. Davenport’s team and Wood’s team both learnt that they’d been tracking down two different populations of the same monkey in October 2004 – one population in the Mount Rungwe-Livingstone Forest area in the Southern Highlands of Tanzania, and the other in the Ndundulu Forest Reserve in the Tanzanian Udzungwa Mountains.

In May 2005 they published a jointly authored description of this new species in Science (Jones et al. 2005), naming it the Highland mangabey Lophocebus kipunji Ehardt, Butynski, Jones & Davenport, 2005. Note that the authorship of the species doesn’t match the authorship of the descriptive paper. This does happen occasionally in the literature, and in this case it means that three authors of the original description were not involved in the naming of the species. Something else makes the Jones et al. paper odd, however, and this is the apparent lack of a type specimen for Lophocebus kipunji. Nowhere in the paper do they list or cite an accessioned specimen, nor mention the procurement of a specimen for a museum or university collection. Under ‘holotype’ they wrote ‘Adult male in photograph (Fig. 2)’, with a ‘paratype’ being described as ‘Adult in photograph (Fig. 3)’ (p. 1162). Because the new species seems to be critically endangered, Jones et al. (2005, p. 1162) stated ‘no live individual should be collected at this time to serve as the holotype’.

While it might seem ethically ‘nice’ and – from the conservationist perspective – sensible to not collect specimens from endangered or declining populations, it’s problematic to not do so, as the ICZN mandates that actual type specimens are needed for the establishment of a species. Furthermore, biological entities can only be regarded as unquestionably valid when there are physical specimens accessioned in proper collections.

Consequently there were several follow-up comments in Science on the lack of a Highland mangabey holotype (Landry 2005, Moser 2005, Polaszek et al. 2005, Timm et al. 2005). Timm et al. (2005) argued that the lack of a type specimen means that Lophocebus kipunji ‘is not an available name and has no formal standing in zoology’ (p. 2163) and Landry (2005) argued that the authors should have published ‘all of the excellent descriptive material and their quite convincing case for calling it new, without, however, naming it’ (p. 2164). Landry also noted that only four of the seven authors of the paper are listed as namers of the new species, but that ‘the purpose of this citation is to identify the paper, not to assign credit, and all of the authors should be cited’. Interesting.

Polaszek et al. (2005) responded to these criticisms by arguing that the ICZN does actually allow the recognition of taxa without holotypes (Article 73.1.4), and they argued that conservation concerns should encourage zoologists to catalogue species on the basis of vocalisations, molecular information and so on, and that ‘dead animal specimens should not be understood to be essential to the process of establishing new taxa’ (p. 2165). Hell, if Bernard Heuvelmans were still alive he would dance a little jig (to paraphrase Greg Paul). Moser (2005) pointed out that Polaszek et al. (2005) seem to have completely misunderstood the point of Article 73.1.4: it refers to cases where type specimens have become lost, and does NOT say that lack of an original type specimen is acceptable.

Anyway, it isn’t the first time that this has happened, and it won’t be the last. Among tetrapods the most famous case is that of the Bulo Burti boubou Laniarius liberatus, a Somalian shrike captured, observed in captivity, and then released (Smith et al. 1991). Exactly the same thing has just happened with another new monkey: a Brazilian platyrrhine named the Blond capuchin Cebus quierozi Mendes Pontes & Malta, 2006 (again, the species’ authorship doesn’t match the authorship of the paper. Again, weird). Apparently critically endangered and restricted to a tiny area already renowned as a centre of endemism, the authors elected not to sacrifice the type specimen (ironically confiscated from a local hunter), but to release it back into the wild (Mendes Pontes et al. 2006). I could talk about this subject a lot more, but won’t do so here. Suffice it to say, I still think that the collection of specimens is an integral part of zoological science (see Patterson 2002). Naming species on the basis of photos, vocalizations and molecular data alone opens the door for the official recognition of taxa that most zoologists are not ready to accept: on these grounds, Sasquatch is clearly a valid, nameable taxon for example.

To get back to the Highland mangabey, the problematic lack of a type specimen is now an academic argument, as a museum-accessioned specimen has been procured: it is a sub-adult male found dead in a trap in August 2005, currently accessioned at the Field Museum of Natural History, Chicago. It possesses the diagnostic features of the specimens previously described as representing this species, so seems to be securely and correctly identified (note here one of the practical problems of lacking a holotype: we don’t have a physical specimen that we can compare latterly obtained specimens to). The Chicago specimen is significant, as study of its DNA sequence data has provided new information on the affinities and evolution of the Highland mangabey, and on mangabeys and their relatives as a whole.

About Me

Darren Naish is a science writer, technical editor and palaeozoologist (affiliated with the University of Southampton, UK). He mostly works on Cretaceous dinosaurs and pterosaurs but has an avid interest in all things tetrapod. His publications can be downloaded at darrennaish.wordpress.com. He has been blogging at Tetrapod Zoology since 2006. YOU ARE CURRENTLY AT A VERY OLD VERSION OF TET ZOO: for modern articles, go to: http://blogs.scientificamerican.com/tetrapod-zoology/ And check out the Tet Zoo podcast at tetzoo.com!